14.12 How pathogens attack plants

Pathogens need to invade their hosts in order to cause disease and assure
their own survival, so they are equipped with mechanisms for attachment,
identification and invasion of suitable hosts. Entering the host tissues
might involve finding and entering through an existing aperture, such as a stoma
or an injury, or direct mechanical attack. How do they find the right place to
invade?

A spore that alights on a leaf surface adheres to that surface by
hydrophobic interactions between hydrophobins in the spore wall and the
hydrophobic surface of the leaf cuticle (see the section entitled On the far
side in Chapter 6; CLICK HERE to
view the page). The hypha that emerges from the spore senses an appropriate site
and when it finds it, the hyphal tip enlarges (differentiating into an
appressorium) and strengthens the adhesion to the leaf surface. A
strong hold on the leaf surface is necessary to support the amount of mechanical
force used to penetrate into the plant.

Growth of conidial germ tubes of these pathogens on leaves or artificial
substrates is usually perpendicular to ridges and furrows on the surface. Ridges
or grooves 0.5 µm high by 2.0 µm wide in artificial surfaces induce appressorium
formation within four minutes after contact. This is a thigmotropism,
a directional growth in response to touch or physical contact stimuli with a
solid object; a similar mechanism operates in animal pathogens also also
although there are some subtle differences in the mechanism (Nikawa et al.,
1997; Stephenson et al., 2014).

In plant pathogens, the object with which the fungus is interacting is the
plant cuticle, which is external to the cell and on the surface of the cell wall
of external, usually epidermal, cells. Components of the cuticle are in layers
in a matrix of cutin. The outer surface is mainly, or only,
composed of very hydrophobic waxes, with the inner layers,
those closest to the epidermal cell wall, being very hydrophilic
(cellulose-rich) in composition. This shift from hydrophilic to hydrophobic
between inner and outer surface provides the plant with a uniform protective
barrier that retards moisture loss from the plant cell surface. The growing
hypha is able to sense very minute alterations in the surface texture and the
spacing between ridges on the natural leaf surface such as those that occur
between epidermal cells and especially around stoma. Extension growth of the
germ tube hypha ceases after its apex has grown over a stomatal guard-cell lip
(or a depression on an artificial surface in vitro) and the
appressorium is formed over the stoma
(Łaźniewska et al., 2012; Bellincampi et al., 2014; Serrano
et al., 2014).

Thigmotropism is not the only surface cue involved in plant
pathogens; surface hardness and, separately, surface hydrophobicity stimuli are
essential for appressorium formation and differentiation in the rice blast
fungus Magnaporthe oryzae. The pathogen employs a series of receptors
and sensors at the plasma membrane to recognise host surface cues and to
activate signal transduction pathways required for appressorium formation and
pathogenicity.

The rice blast fungus senses chemical cues from
primary alcohols, which are major component of leaf waxes in grasses, while
other fungal sensors recognise hydrophobicity and precursors of cutin
molecules on rice leaves. Fungal endocytosis is responsible for
internalising the signals and triggering regulators of G-protein signalling
cascades, accumulation of cAMP, MAPK pathway proteins, and inducing
chitin-deacetylase activity, which is necessary for appressorium formation
(Liu et al., 2007; Liuet al., 2011; Kuroki et al., 2017; Li et al.,
2017). Additionally, there are indications that these mycelia also respond
chemotropically to the stomata, presumably to the
gases emerging from the substomatal space.